Cryptic diversity of cellulose-degrading gut bacteria in industrialized humans
Humans, like all mammals, depend on the gut microbiome for digestion of cellulose, the main component of plant fiber. However, evidence for cellulose fermentation in the human gut is scarce. We have identified ruminococcal species in the gut microbiota of human populations that assemble functional m...
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| Published in | Science (American Association for the Advancement of Science) Vol. 383; no. 6688; p. eadj9223 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
15.03.2024
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0036-8075 1095-9203 1095-9203 |
| DOI | 10.1126/science.adj9223 |
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| Abstract | Humans, like all mammals, depend on the gut microbiome for digestion of cellulose, the main component of plant fiber. However, evidence for cellulose fermentation in the human gut is scarce. We have identified ruminococcal species in the gut microbiota of human populations that assemble functional multienzymatic cellulosome structures capable of degrading plant cell wall polysaccharides. One of these species, which is strongly associated with humans, likely originated in the ruminant gut and was subsequently transferred to the human gut, potentially during domestication where it underwent diversification and diet-related adaptation through the acquisition of genes from other gut microbes. Collectively, these species are abundant and widespread among ancient humans, hunter-gatherers, and rural populations but are rare in populations from industrialized societies thus indicating potential disappearance in response to the westernized lifestyle.
The guts of urbanized people worldwide are known to contain less microbial biodiversity than those of humans living rurally. The worry is that the loss of key species contributes to the increasing prevalence of poor metabolic health among urbanized people. By searching for key genes involved in cellulose degradation in metagenome-assembled genomes, Moraïs
et al
. discovered cellulolytic bacteria in humans. All candidate
Ruminococcus
species assembled active cellulosomes, enzyme complexes capable of degrading microcrystalline cellulose. Three species were distinguished with phylogenies indicating derivation from primate and ruminant hosts, and they showed specific host preferences and ongoing host adaptation. The occurrence of cellulolytic bacteria in humans reveals that a complicated process of dynamic co-evolution occurs in the gut and is possibly regulated by environment. —Caroline Ash
Cellulolytic human gut bacteria are scarce in urban societies but abundant in ancient and hunter-gatherer microbiomes. |
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| AbstractList | Humans, like all mammals, depend on the gut microbiome for digestion of cellulose, the main component of plant fiber. However, evidence for cellulose fermentation in the human gut is scarce. We have identified ruminococcal species in the gut microbiota of human populations that assemble functional multienzymatic cellulosome structures capable of degrading plant cell wall polysaccharides. One of these species, which is strongly associated with humans, likely originated in the ruminant gut and was subsequently transferred to the human gut, potentially during domestication where it underwent diversification and diet-related adaptation through the acquisition of genes from other gut microbes. Collectively, these species are abundant and widespread among ancient humans, hunter-gatherers, and rural populations but are rare in populations from industrialized societies thus indicating potential disappearance in response to the westernized lifestyle.
The guts of urbanized people worldwide are known to contain less microbial biodiversity than those of humans living rurally. The worry is that the loss of key species contributes to the increasing prevalence of poor metabolic health among urbanized people. By searching for key genes involved in cellulose degradation in metagenome-assembled genomes, Moraïs
et al
. discovered cellulolytic bacteria in humans. All candidate
Ruminococcus
species assembled active cellulosomes, enzyme complexes capable of degrading microcrystalline cellulose. Three species were distinguished with phylogenies indicating derivation from primate and ruminant hosts, and they showed specific host preferences and ongoing host adaptation. The occurrence of cellulolytic bacteria in humans reveals that a complicated process of dynamic co-evolution occurs in the gut and is possibly regulated by environment. —Caroline Ash
Cellulolytic human gut bacteria are scarce in urban societies but abundant in ancient and hunter-gatherer microbiomes. Humans, like all mammals, depend on the gut microbiome for digestion of cellulose, the main component of plant fiber. However, evidence for cellulose fermentation in the human gut is scarce. We have identified ruminococcal species in the gut microbiota of human populations that assemble functional multienzymatic cellulosome structures capable of degrading plant cell wall polysaccharides. One of these species, which is strongly associated with humans, likely originated in the ruminant gut and was subsequently transferred to the human gut, potentially during domestication where it underwent diversification and diet-related adaptation through the acquisition of genes from other gut microbes. Collectively, these species are abundant and widespread among ancient humans, hunter-gatherers, and rural populations but are rare in populations from industrialized societies thus indicating potential disappearance in response to the westernized lifestyle. Editor’s summaryThe guts of urbanized people worldwide are known to contain less microbial biodiversity than those of humans living rurally. The worry is that the loss of key species contributes to the increasing prevalence of poor metabolic health among urbanized people. By searching for key genes involved in cellulose degradation in metagenome-assembled genomes, Moraïs et al. discovered cellulolytic bacteria in humans. All candidate Ruminococcus species assembled active cellulosomes, enzyme complexes capable of degrading microcrystalline cellulose. Three species were distinguished with phylogenies indicating derivation from primate and ruminant hosts, and they showed specific host preferences and ongoing host adaptation. The occurrence of cellulolytic bacteria in humans reveals that a complicated process of dynamic co-evolution occurs in the gut and is possibly regulated by environment. —Caroline AshINTRODUCTIONMammals, including humans, rely on their gut’s microbial community to break down plant cell wall components, notably cellulose and associated polysaccharides. However, there is limited evidence for cellulose fermentation in the human gut despite the benefits of cellulose-containing dietary fiber for gut-microbiome health and overall human well-being.RATIONALEBy investigating the presence of heretofore undescribed bacterial species within the human-gut microbiota that degrade complex cellulosic polysaccharides, we can reveal their potential sources and understand their intricate adaptations to diverse host lifestyles and diets. Insight into the prevalence and abundance of these bacteria across diverse mammalian species and a wide range of human populations will provide critical knowledge of their evolutionary origins, ancestral associations, and trajectories that enabled their incorporation into the human gut.RESULTSPreviously unknown ruminococcal species were discovered in the human-gut microbiota and provisionally named Candidatus Ruminococcus primaciens, Ruminococcus hominiciens, and Ruminococcus ruminiciens, all of which assemble functional multienzymatic cellulosome systems that degrade crystalline cellulose. These species are prevalent among the great apes and other nonhuman primates, ancient human societies, hunter-gatherer communities, and rural populations. Although widespread geographically they are conspicuously rare within industrialized societies. Notably, they exhibit distinct host preferences wherein R. hominiciens is associated primarily with humans and great apes and R. primaciens predominantly inhabits the gut of nonhuman primates and ancient human populations. Moreover, these species display host-specific diversification, forming distinct clades within the phylogenetic tree and aligning with their respective hosts. Our evolutionary analysis strongly suggests that R. hominiciens likely originated in the ruminant gut and later transferred to humans, possibly during domestication. High gene expression levels were observed for these species, reflecting their considerable activity in their respective gut systems. Furthermore, their gene expression profile aligns with their hosts’ dietary preferences, highlighting their adaptability. Our analyses show that these novel species adapt to their host ecosystems by acquiring genes from co-resident gut microbes. The human-associated strains possess functional adaptability highlighted by the acquisition of genes that can degrade specific plant fibers of monocots such as maize, rice, and wheat—major components of the human diet. Likewise, the nonhuman primate–associated strain exhibits the potential for degrading chitin, a polymer abundant in the insect exoskeleton, part of the diet of nonhuman primates. Our data provide insight into the ongoing colonization of these species within the human gut, particularly those originating from ruminants and nonhuman primates. Specific strains appear to represent intermediates between primate- and rumen-gut ecosystems, as evidenced by their gene content during establishment in the human intestine.CONCLUSIONOur accumulated data indicate that ruminococcal lineages were more widespread in the past, evidenced by the high prevalence and abundance of these strains in ancient human populations and among hunter gatherer communities and rural societies, combined with their global distribution and low prevalence in industrialized societies. Differences in their prevalence among human populations may reflect dietary variation between industrialized and nonindustrialized societies. Dietary fiber intake appears to be a key factor as high-fiber diets are reported among Hadza hunter-gatherers whereas lower fiber intake is observed in rural populations and the least consumption of fiber occurs in industrialized societies. These findings collectively imply a decline of these species in the human gut, likely influenced by the shift toward westernized lifestyles, potentially impacting energy balance and other health-related aspects. The presence of transitional strains that recently colonized the human gut indicates that ruminants and nonhuman primates could be a source and reservoir for cellulosome-producing ruminococcal strains, which continue to colonize and adapt to the human gut. There may be potential for intentional reintroduction or enrichment of these species in the human gut through targeted dietary approaches and specialized probiotics. Humans, like all mammals, depend on the gut microbiome for digestion of cellulose, the main component of plant fiber. However, evidence for cellulose fermentation in the human gut is scarce. We have identified ruminococcal species in the gut microbiota of human populations that assemble functional multienzymatic cellulosome structures capable of degrading plant cell wall polysaccharides. One of these species, which is strongly associated with humans, likely originated in the ruminant gut and was subsequently transferred to the human gut, potentially during domestication where it underwent diversification and diet-related adaptation through the acquisition of genes from other gut microbes. Collectively, these species are abundant and widespread among ancient humans, hunter-gatherers, and rural populations but are rare in populations from industrialized societies thus indicating potential disappearance in response to the westernized lifestyle.Humans, like all mammals, depend on the gut microbiome for digestion of cellulose, the main component of plant fiber. However, evidence for cellulose fermentation in the human gut is scarce. We have identified ruminococcal species in the gut microbiota of human populations that assemble functional multienzymatic cellulosome structures capable of degrading plant cell wall polysaccharides. One of these species, which is strongly associated with humans, likely originated in the ruminant gut and was subsequently transferred to the human gut, potentially during domestication where it underwent diversification and diet-related adaptation through the acquisition of genes from other gut microbes. Collectively, these species are abundant and widespread among ancient humans, hunter-gatherers, and rural populations but are rare in populations from industrialized societies thus indicating potential disappearance in response to the westernized lifestyle. |
| Author | Kapust, Nils Martin, William F. Levin, Liron Nagies, Falk S. P. Moraïs, Sarah Yadav, Madhav P. Artan-Furman, Avital Zorea, Alvah Bayer, Edward A. Lamed, Eva Bolam, David N. Winkler, Sarah Mizrahi, Itzhak |
| Author_xml | – sequence: 1 givenname: Sarah orcidid: 0000-0001-9026-2386 surname: Moraïs fullname: Moraïs, Sarah organization: National Institute of Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer-Sheva, 84105, Israel., Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel., The Goldman Sonnenfeldt School of Sustainability and Climate Change, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel – sequence: 2 givenname: Sarah orcidid: 0000-0002-6675-9939 surname: Winkler fullname: Winkler, Sarah organization: National Institute of Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer-Sheva, 84105, Israel., Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel., The Goldman Sonnenfeldt School of Sustainability and Climate Change, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel – sequence: 3 givenname: Alvah orcidid: 0000-0001-6543-2259 surname: Zorea fullname: Zorea, Alvah organization: National Institute of Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer-Sheva, 84105, Israel., Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel., The Goldman Sonnenfeldt School of Sustainability and Climate Change, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel – sequence: 4 givenname: Liron orcidid: 0009-0003-1591-7903 surname: Levin fullname: Levin, Liron organization: Bioinformatics Core Facility, llse Katz Institute for Nanoscale Science and Technology, Ben-Gurion University of the Negev, Beer-Sheva, Israel – sequence: 5 givenname: Falk S. P. surname: Nagies fullname: Nagies, Falk S. P. organization: Department of Biology, Institute for Molecular Evolution, Heinrich-Heine-Universität Düsseldorf, D-40225, Düsseldorf, Germany – sequence: 6 givenname: Nils orcidid: 0000-0001-8178-254X surname: Kapust fullname: Kapust, Nils organization: Department of Biology, Institute for Molecular Evolution, Heinrich-Heine-Universität Düsseldorf, D-40225, Düsseldorf, Germany – sequence: 7 givenname: Eva surname: Lamed fullname: Lamed, Eva organization: Department of Biomolecular Sciences, The Weizmann Institute of Science, Rehovot 7610001 Israel – sequence: 8 givenname: Avital surname: Artan-Furman fullname: Artan-Furman, Avital organization: Department of Biomolecular Sciences, The Weizmann Institute of Science, Rehovot 7610001 Israel – sequence: 9 givenname: David N. orcidid: 0000-0003-0314-3122 surname: Bolam fullname: Bolam, David N. organization: Institute for Cell and Molecular Biosciences, The Medical School, Newcastle University, Newcastle upon Tyne, NE2 4HH, UK – sequence: 10 givenname: Madhav P. surname: Yadav fullname: Yadav, Madhav P. organization: US Department of Agriculture, Agricultural Research Service, Eastern Regional Research Center, 600 East Mermaid Lane, Wyndmoor, PA 19038, USA – sequence: 11 givenname: Edward A. surname: Bayer fullname: Bayer, Edward A. organization: National Institute of Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer-Sheva, 84105, Israel., Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel., Department of Biomolecular Sciences, The Weizmann Institute of Science, Rehovot 7610001 Israel – sequence: 12 givenname: William F. orcidid: 0000-0003-1478-6449 surname: Martin fullname: Martin, William F. organization: Department of Biology, Institute for Molecular Evolution, Heinrich-Heine-Universität Düsseldorf, D-40225, Düsseldorf, Germany – sequence: 13 givenname: Itzhak orcidid: 0000-0001-6636-8818 surname: Mizrahi fullname: Mizrahi, Itzhak organization: National Institute of Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer-Sheva, 84105, Israel., Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel., The Goldman Sonnenfeldt School of Sustainability and Climate Change, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel |
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| Snippet | Humans, like all mammals, depend on the gut microbiome for digestion of cellulose, the main component of plant fiber. However, evidence for cellulose... Editor’s summaryThe guts of urbanized people worldwide are known to contain less microbial biodiversity than those of humans living rurally. The worry is that... |
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| SubjectTerms | Adaptability Apes Bacteria Bioaccumulation Biodiversity Cell walls Cellulolytic bacteria Cellulose Cellulose - metabolism Cellulose fibers cellulosome Cellulosomes Chitin Coevolution Crystalline cellulose Degradation Diet Dietary fiber Dietary Fiber - metabolism Dietary intake digestion Digestive system Domestication Ecosystems Energy balance Evolution Exoskeleton Exoskeletons Fermentation Food intake Gastrointestinal Microbiome - genetics Gastrointestinal Microbiome - physiology Gastrointestinal tract Gene expression Genes Genomes Host preferences Human populations Humans Industrial Development industrialization Insects Intermediates Intestinal microflora intestinal microorganisms Intestine lifestyle Mammals Microbiota Microorganisms Monkeys & apes Phylogeny Plant fibers Polymers Polysaccharides Populations Preferences Primates Probiotics Reintroduction ruminants Ruminococcus Ruminococcus - classification Ruminococcus - enzymology Ruminococcus - genetics Rural populations Saccharides Species Vegetable fibers Well being |
| Title | Cryptic diversity of cellulose-degrading gut bacteria in industrialized humans |
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